Mechanosensitive ATP release maintains proper mucus hydration of airways

Science Signaling

Volumn 6, Issue 279, 2013, Pages

  Button, Brian ^a,b   Okada, Seiko F ^a,b   Frederick, Charles Brandon ^b   Thelin, William R ^c   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c Parion Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ADENOSINE TRIPHOSPHATE; DENUFOSOL; DEOXYCYTIDINE PHOSPHATE; PURINERGIC P2Y RECEPTOR AGONIST; PURINERGIC P2Y2 RECEPTOR; URIDINE; WATER;

ARTICLE; BRONCHUS MUCOSA; BRONCHUS MUCUS; CELL STIMULATION; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HYDRATION; MECHANICAL STRESS; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; VISCOELASTICITY; ANALOGS AND DERIVATIVES; BIOLOGICAL MODEL; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; ELASTICITY; EPITHELIUM; EPITHELIUM CELL; EXTRACELLULAR FLUID; INTRACELLULAR FLUID; METABOLISM; MUCOCILIARY CLEARANCE; MUCUS; RESPIRATORY SYSTEM; RESPIRATORY TRACT MUCOSA; SECRETION (PROCESS); VISCOSITY;

ADENOSINE; ADENOSINE TRIPHOSPHATE; CELLS, CULTURED; CILIA; DEOXYCYTOSINE NUCLEOTIDES; ELASTICITY; EPITHELIAL CELLS; EPITHELIUM; EXTRACELLULAR FLUID; HUMANS; INTRACELLULAR FLUID; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUCOCILIARY CLEARANCE; MUCUS; PURINERGIC P2Y RECEPTOR AGONISTS; RECEPTORS, PURINERGIC P2Y2; RESPIRATORY MUCOSA; RESPIRATORY SYSTEM; STRESS, MECHANICAL; URIDINE; VISCOSITY; WATER;

EID: 84879974863     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003755     Document Type: Article

References (53)

1. S. H. Randell, R. C. Boucher, University of North Carolina Virtual Lung Group, Effective mucus clearance is essential for respiratory health. Am. J. Respir. Cell Mol. Biol. 35, 20-28 (2006).
2. D. Paisley, M. Gosling, H. Danahay, Regulation of airway mucosal hydration. Expert Rev. Clin. Pharmacol. 3, 361-369 (2010).
3. B. Xia, J. A. Royall, G. Damera, G. P. Sachdev, R. D. Cummings, Altered O-glycosylation and sulfation of airway mucins associated with cystic fibrosis. Glycobiology 15, 747-775 (2005).
4. S. M. Kreda, C. W. Davis, M. C. Rose, CFTR, mucins, and mucus obstruction in cystic fibrosis. Cold Spring Harb. Perspect. Med. 2, a009589 (2012).
5. P. M. Quinton, Role of epithelial HCO3 - transport in mucin secretion: Lessons from cystic fibrosis. Am. J. Physiol. Cell Physiol. 299, C1222-C1233 (2010).
6. R. C. Boucher, Airway surface dehydration in cystic fibrosis: Pathogenesis and therapy. Annu. Rev. Med. 58, 157-170 (2007).
7. H. Castrop, Mediators of tubuloglomerular feedback regulation of glomerular filtration: ATP and adenosine. Acta Physiol. 189, 3-14 (2007).
8. L. M. Satlin, M. D. Carattino, W. Liu, T. R. Kleyman, Regulation of cation transport in the distal nephron by mechanical forces. Am. J. Physiol. Renal Physiol. 291, F923-F931 (2006).
9. R. Tarran, B. Button, M. Picher, A. M. Paradiso, C. M. Ribeiro, E. R. Lazarowski, L. Zhang, P. L. Collins, R. J. Pickles, J. J. Fredberg, R. C. Boucher, Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J. Biol. Chem. 280, 35751-35759 (2005).
10. B. Button, M. Picher, R. C. Boucher, Differential effects of cyclic and constant stress on ATP release and mucociliary transport by human airway epithelia. J. Physiol. 580, 577-592 (2007).
11. J. L. Salisbury, Primary cilia: Putting sensors together. Curr. Biol. 14, R765-R767 (2004).
12. H. A. Praetorius, K. R. Spring, The renal cell primary cilium functions as a flow sensor. Curr. Opin. Nephrol. Hypertens. 12, 517-520 (2003).
13. R. Jain, J. Pan, J. A. Driscoll, J.W.Wisner, T. Huang, S. P. Gunsten, Y. You, S. L. Brody, Temporal relationship between primary and motile ciliogenesis in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 43, 731-739 (2010).
14. H. Matsui, B. R. Grubb, R. Tarran, S. H. Randell, J. T. Gatzy, C.W. Davis, R. C. Boucher, Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95, 1005-1015 (1998).
15. R. Tarran, Regulation of airway surface liquid volume and mucus transport by active ion transport. Proc. Am. Thorac. Soc. 1, 42-46 (2004).
16. A. J. Hirsh, J. R. Stonebraker, C. A. van Heusden, E. R. Lazarowski, R. C. Boucher, M. Picher, Adenosine deaminase 1 and concentrative nucleoside transporters 2 and 3 regulate adenosine on the apical surface of human airway epithelia: Implications for inflammatory lung diseases. Biochemistry 46, 10373-10383 (2007).
17. E. R. Lazarowski, R. Tarran, B. R. Grubb, C. A. van Heusden, S. Okada, R. C. Boucher, Nucleotide release provides a mechanism for airway surface liquid homeostasis. J. Biol. Chem. 279, 36855-36864 (2004).
18. B. Button, R. C. Boucher, University of North Carolina Virtual Lung Group, Role of mechanical stress in regulating airway surface hydration and mucus clearance rates. Respir. Physiol. Neurobiol. 163, 189-201 (2008).
19. M. Kesimer, S. Kirkham, R. J. Pickles, A. G. Henderson, N. E. Alexis, G. Demaria, D. Knight, D. J. Thornton, J. K. Sheehan, Tracheobronchial air-liquid interface cell culture: A model for innate mucosal defense of the upper airways? Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L92-L100 (2009).
20. B. Button, L. H. Cai, C. Ehre, M. Kesimer, D. B. Hill, J. K. Sheehan, R. C. Boucher, M. Rubinstein, A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337, 937-941 (2012).
21. H. Matsui, V. E.Wagner, D. B. Hill, U. E. Schwab, T. D. Rogers, B. Button, R. M. Taylor II, R. Superfine, M. Rubinstein, B. H. Iglewski, R. C. Boucher, A physical linkage between cystic fibrosis airway surface dehydration and Pseudomonas aeruginosa biofilms. Proc. Natl. Acad. Sci. U.S.A. 103, 18131-18136 (2006).
22. J. J. Fredberg, A modal perspective of lung response. J. Acoust. Soc. Am. 63, 962-966 (1978).
23. M. Meeks, A. Bush, Primary ciliary dyskinesia (PCD). Pediatr. Pulmonol. 29, 307-316 (2000).
24. M. W. Martin, T. K. Harden, Agonist-induced desensitization of a P2Y-purinergic receptorregulated phospholipase C. J. Biol. Chem. 264, 19535-19539 (1989).
25. B. R. Yerxa, J. R. Sabater, C. W. Davis, M. J. Stutts, M. Lang-Furr, M. Picher, A. C. Jones, M. Cowlen, R. Dougherty, J. Boyer, W. M. Abraham, R. C. Boucher, Pharmacology of INS37217 [P1-(uridine 5′)-P4- (2′-deoxycytidine 5′)tetraphosphate, tetrasodium salt], a next-generation P2Y2 receptor agonist for the treatment of cystic fibrosis. J. Pharmacol. Exp. Ther. 302, 871-880 (2002).
26. K. Kunzelmann, T. Bachhuber, R. Regeer, D. Markovich, J. Sun, R. Schreiber, Purinergic inhibition of the epithelial Na+ transport via hydrolysis of PIP2. FASEB J. 19, 142-143 (2005).
27. R. C. Boucher, Regulation of airway surface liquid volume by human airway epithelia. Pflugers Arch. 445, 495-498 (2003).
28. B. R. Grubb, R. C. Boucher, Effect of in vivo corticosteroids on Na+ transport across airway epithelia. Am. J. Physiol. 275, C303-C308 (1998).
29. K. Yamamoto, R. Korenaga, A. Kamiya, J. Ando, Fluid shear stress activates Ca2+ influx into human endothelial cells via P2X4 purinoceptors. Circ. Res. 87, 385-391 (2000).
30. D. C. Genetos, D. J. Geist, D. Liu, H. J. Donahue, R. L. Duncan, Fluid shear-induced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J. Bone. Miner. Res. 20, 41-49 (2005).
31. P. Bodin, D. Bailey, G. Burnstock, Increased flow-induced ATP release from isolated vascular endothelial cells but not smooth muscle cells.Br. J. Pharmacol. 103, 1203-1205 (1991).
32. P. T. Schumacker, Straining to understand mechanotransduction in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L881-L882 (2002).
33. W. A. Price, A. D. Stiles, New insights into lung growth and development. Curr. Opin. Pediatr. 8, 202-208 (1996).
34. J. Pan, I. Copland, M. Post, H. Yeger, E. Cutz, Mechanical stretch-induced serotonin release from pulmonary neuroendocrine cells: Implications for lung development. Am. J. Physiol. Lung Cell. Mol. Physiol. 290, L185-L193 (2006).
35. R. Grygorczyk, J. W. Hanrahan, CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. Am. J. Physiol. 272, C1058-C1066 (1997).
36. L. Homolya, T. H. Steinberg, R. C. Boucher, Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J. Cell Biol. 150, 1349-1360 (2000).
37. A. Guyot, J. W. Hanrahan, ATP release from human airway epithelial cells studied using a capillary cell culture system. J. Physiol. 545, 199-206 (2002).
38. W. Liu, S. Xu, C. Woda, P. Kim, S. Weinbaum, L. M. Satlin, Effect of flow and stretch on the [Ca2+]i response of principal and intercalated cells in cortical collecting duct. Am. J. Physiol. Renal Physiol. 285, F998-F1012 (2003).
39. W. Möller, K. Häussinger, L. Ziegler-Heitbrock, J. Heyder, Mucociliary and long-term particle clearance in airways of patients with immotile cilia. Respir. Res. 7, 10 (2006).
40. P. J. Basser, T. A. McMahon, P. Griffith, The mechanism of mucus clearance in cough. J. Biomech. Eng. 111, 288-297 (1989).
41. M. I. Lethem, S. L. James, C. Marriott, J. F. Burke, The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur. Respir. J. 3, 19-23 (1990).
42. D. A. Groneberg, P. R. Eynott, T. Oates, S. Lim, R. Wu, I. Carlstedt, A. G. Nicholson, K. F. Chung, Expression of MUC5AC and MUC5B mucins in normal and cystic fibrosis lung. Respir. Med. 96, 81-86 (2002).
43. M. O. Henke, G. John, C. Rheineck, S. Chillappagari, L. Naehrlich, B. K. Rubin, Serine proteases degrade airway mucins in cystic fibrosis. Infect. Immun. 79, 3438-3444 (2011).
44. P. W. Cheng, T. F. Boat, K. Cranfill, J. R. Yankaskas, R. C. Boucher, Increased sulfation of glycoconjugates by cultured nasal epithelial cells from patients with cystic fibrosis. J. Clin. Invest. 84, 68-72 (1989).
45. A. Piccini, S. Carta, S. Tassi, D. Lasiglié, G. Fossati, A. Rubartelli, ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1b and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. U.S.A. 105, 8067-8072 (2008).
46. E. R. Lazarowski, R. C. Boucher, Purinergic receptors in airway epithelia. Curr. Opin. Pharmacol. 9, 262-267 (2009).
47. L. M. Satlin, S. Sheng, C. B. Woda, T. R. Kleyman, Epithelial Na+ channels are regulated by flow. Am. J. Physiol. Renal Physiol. 280, F1010-F1018 (2001).
48. A. Garcia-Caballero, J. E. Rasmussen, E. Gaillard,M. J.Watson, J. C. Olsen, S. H. Donaldson, M. J. Stutts, R. Tarran, SPLUNC1 regulates airway surface liquid volume by protecting ENaC from proteolytic cleavage. Proc. Natl. Acad. Sci. U.S.A. 106, 11412-11417 (2009).
49. E. R. Lazarowski, R. C. Boucher, T. K. Harden, Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64, 785-795 (2003).
50. G. A. Ransford, N. Fregien, F. Qiu, G. Dahl, G. E. Conner, M. Salathe, Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41, 525-534 (2009).
51. M. L. Fulcher, S. Gabriel, K. A. Burns, J. R. Yankaskas, S. H. Randell, Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107, 183-206 (2005).
52. R. Tarran, R. C. Boucher, Thin-film measurements of airway surface liquid volume/ composition and mucus transport rates in vitro. Methods Mol. Med. 70, 479-492 (2002).
53. J. H. Sisson, J. A. Stoner, B. A. Ammons, T. A. Wyatt, All-digital image capture and whole-field analysis of ciliary beat frequency. J. Microsc. 211, 103-111 (2003).